Non-invasive hydrodynamic imaging in plant roots at cellular resolution

Pascut, Flavius C.; Couvreur, Valentin; Dietrich, Daniela; Leftley, Nicky; Reyt, Guilhem; Boursiac, Yann; Calvo-Polanco, Mónica; Casimiro, Ilda; Maurel, Christophe; Salt, David E.; Wells, Darren M.; Bennett, Malcolm; Webb, Kevin F.

doi:10.1038/s41467-021-24913-z

Cited by 31 publications

(19 citation statements)

References 43 publications

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“…Our major concern was to understand the relative impact of elementary axial and radial hydraulic parameters on sap flow. Whereas confrontation of theoretical and experimental data through model sensitivity analysis remains the most common approach, there is a restricted number of studies whereby hydraulic parameters were deduced from inverse modeling and integration of architectural components ( Doussan et al, 1998b , 2006 ; Zarebanadkouki et al, 2016; Meunier et al, 2018 ; Pascut et al, 2021 ;). While these earlier studies relied on functional analyses of individual axial roots of maize, lupine or Arabidopsis, we describe here a procedure based on cut-and-flow measurements for simultaneous determination of axial and radial conductance in highly branched root systems.…”

Section: Discussionmentioning

confidence: 99%

Phenotyping and modeling of root hydraulic architecture reveal critical determinants of axial water transport

et al. 2022

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Water uptake by roots is a key adaptation of plants to aerial life. Water uptake depends on root system architecture (RSA) and tissue hydraulic properties that, together, shape the root hydraulic architecture. This work investigates how the interplay between conductivities along radial (e.g. aquaporins) and axial (e.g. xylem vessels) pathways determines the water transport properties of highly branched RSAs as found in adult Arabidopsis (Arabidopsis thaliana) plants. A hydraulic model named HydroRoot was developed, based on multi-scale tree graph representations of RSAs. Root water flow was measured by the pressure chamber technique after successive cuts of a same root system from the tip towards the base. HydroRoot model inversion in corresponding RSAs allowed us to concomitantly determine radial and axial conductivities, providing evidence that the latter is often overestimated by classical evaluation based on the Hagen-Poiseuille law. Organizing principles of Arabidopsis primary and lateral root growth and branching were determined and used to apply the HydroRoot model to an extended set of simulated RSAs. Sensitivity analyses revealed that water transport can be co-limited by radial and axial conductances throughout the whole RSA. The number of roots that can be sectioned (intercepted) at a given distance from the base was defined as an accessible and informative indicator of RSA. The overall set of experimental and theoretical procedures was applied to plants mutated in ESKIMO1 and previously shown to have xylem collapse. This approach will be instrumental to dissect the root water transport phenotype of plants with intricate alterations in root growth or transport functions.

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Section: Discussionmentioning

confidence: 99%

Phenotyping and modeling of root hydraulic architecture reveal critical determinants of axial water transport

et al. 2022

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“…They concluded that besides a dominant apoplastic transport across the rhizodermis and cortex, the contribution of the hydraulic conductance of the cell‐to‐cell path to the overall conductance increased significantly from the first layer of the cortex toward the inner layers from 2% to 23%. At the endodermal diffusion barrier, there is increasing evidence that purely apoplastic water transport is excluded (Knipfer & Fricke, 2010; Pascut et al, 2021) while endodermal cell membrane aquaporins largely mediate cell‐to‐cell water flow (Maurel, 1997; Tyerman et al, 1999) and would control up to 70% of the radial conductance prior to suberisation (Couvreur et al, 2018). However, the analysis of cell‐scale factors controlling root radial conductance is complicated by the fact that the conductance of the multiple composite paths vary radially (Ding et al, 2020) and longitudinally with the maturation of diffusion barriers (Hachez et al, 2006; Wang et al, 2019), and depend on the root direct environment and anatomy (Bramley et al, 2009; Heymans et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…They concluded that besides a dominant apoplastic transport across the rhizodermis and cortex, the contribution of the hydraulic conductance of the cell-to-cell path to the overall conductance increased significantly from the first layer of the cortex toward the inner layers from 2% to 23%. At the endodermal diffusion barrier, there is increasing evidence that purely apoplastic water transport is excluded (Knipfer & Fricke, 2010;Pascut et al, 2021) while endodermal cell membrane aquaporins largely mediate cell-to-cell water flow (Maurel, 1997;Tyerman et al, 1999) and would control up to 70% of the radial conductance prior to suberisation (Couvreur et al, 2018). Asterisks denote statistically significant differences between treatments by Student's t test (P <0.05)…”

Section: Short Term Hn Treatment Induces Genotypedependent Changes In...mentioning

confidence: 99%

Exposure to high nitrogen triggered a genotype‐dependent modulation of cell and root hydraulics, which can involve aquaporin regulation

Pou

Hachez

Couvreur

et al. 2022

Physiologia Plantarum

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Root nitrogen acquisition has been proposed to be regulated by mass flow, a process by which water flow brings nutrients to the root surface, depending on a concerted regulation of the root hydraulic properties and stomatal conductance. As aquaporins play an important role in regulating transcellular water flow, we aimed at evaluating the short‐term effect of high nitrogen (HN) availability on the dynamics of hydraulic parameters at both the root and cell level and the regulation of aquaporins. The effect of short‐term HN (8 mM NO3−) treatment was investigated on 12 diverse 15‐day‐old maize genotypes. Root exposure to HN triggered a rapid (<4 h) increase in the root hydraulic conductivity (Lpr) in seven genotypes while no Lpr variation was recorded for the others, allowing the separation of the genotypes into two groups (HN‐responsive and HN‐nonresponsive). A remarkable correlation between Lpr and the cortex cell hydraulic conductivity (Lpc) was observed. However, while differences in gas exchange parameters were also observed, the variations were genotype‐specific and not always correlated with the root hydraulic parameters. We then investigated whether HN‐induced Lpr variations were linked to the activity and regulation of plasma membrane PIP aquaporins. While some changes in PIP mRNA levels were detected, this was not correlated with the protein levels. On the other hand, the rapid variation in Lpr observed in the B73 genotype was correlated with the PIP protein abundance in the plasma membrane, highlighting PIP posttranslational mechanisms in the short‐term regulation of root hydraulic parameters in response to HN treatment.

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“…Mathematical modelling is a powerful tool to better understand roots and rhizosphere processes and to help us identify optimal root phenotypes in contrasting environments (Roose et al ., 2016; Postma et al ., 2017; Pascut et al ., 2021). Functional-structural root architecture models are particularly well suited for such endeavour (Dunbabin et al ., 2013; Landl et al ., 2021).…”

Section: Plant Modelling: An Underused Approach To Root Phenotyping?mentioning

confidence: 99%

A snapshot of the root phenotyping landscape in 2021

Delory

Hernandez‐Soriano

Wacker

et al. 2022

Preprint

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Root phenotyping describes methods for measuring root properties, or traits. While root phenotyping can be challenging, it is advancing quickly. In order for the field to move forward, it is essential to understand the current state and challenges of root phenotyping, as well as the pressing needs of the root biology community. In this letter, we present and discuss the results of a survey that was created and disseminated by members of the Graduate Student and Postdoc Ambassador Program at the 11th symposium of the International Society of Root Research. This survey aimed to (1) provide an overview of the objectives, biological models and methodological approaches used in root phenotyping studies, and (2) identify the main limitations currently faced by plant scientists with regard to root phenotyping. Our survey highlighted that (1) monocotyledonous crops dominate the root phenotyping landscape, (2) root phenotyping is mainly used to quantify morphological and architectural root traits, (3) 2D root scanning/imaging is the most widely used root phenotyping technique, (4) time-consuming tasks are an important barrier to root phenotyping, (5) there is a need for standardised, high-throughput methods to sample and phenotype roots, particularly under field conditions, and to improve our understanding of trait-function relationships.

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Non-invasive hydrodynamic imaging in plant roots at cellular resolution

Cited by 31 publications

References 43 publications

Phenotyping and modeling of root hydraulic architecture reveal critical determinants of axial water transport

Phenotyping and modeling of root hydraulic architecture reveal critical determinants of axial water transport

Exposure to high nitrogen triggered a genotype‐dependent modulation of cell and root hydraulics, which can involve aquaporin regulation

A snapshot of the root phenotyping landscape in 2021

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